Molecular biology of viroid-host interactions and disease control strategies

Plant Science

Volumn 228, Issue , 2014, Pages 48-60

  Kovalskaya, Natalia ^a   Hammond, Rosemarie W ^a  

^a Molecular Plant Pathology Laboratory   (United States)

Author keywords

DsRNA; Resistance; Ribonuclease; Ribozyme; SiRNA; Viroids

Indexed keywords

DISEASE RESISTANCE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; PHYSIOLOGY; PLANT; PLANT DISEASE; PREVENTION AND CONTROL; VIROID; VIROLOGY;

DISEASE RESISTANCE; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANTS; VIROIDS;

EID: 84908330546     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2014.05.006     Document Type: Review

References (232)

1. Diener T.O. Viroids: the smallest known agents of infectious disease. Annu. Rev. Microbiol. 1974, 28:23-40.
2. Martin W.H. "Spindle tuber", a new potato trouble. Hints to potato growers. N. J. State Potato Assoc. 1922, 3(8).
3. Shultz E.S., Folsom D. Transmission, variation and control of certain degeneration diseases of Irish potatoes. J. Agric. Res. 1923, 25:43.
4. Diener T.O., Raymer W.B. Potato spindle tuber virus: a plant virus with properties of a free nucleic acid. Science 1967, 158:378-381.
5. Singh R.P., Clark M.C. Infectious low-molecular weight ribonucleic acid from tomato. Biochem. Biophys. Res. Commun. 1971, 44:1077-1083.
6. Diener T.O. Potato spindle tuber "virus": IV. A replicating, low molecular weight RNA. Virology 1971, 45:411-428.
7. Diener T.O. Discovering viroids - a personal perspective. Nat. Rev. Microbiol. 2003, 1:75-80.
8. Semancik J.S., Weathers L.G. Exocortis disease: an infectious free-nucleic acid plant virus with unusual properties. Virology 1972, 47:456-466.
9. Sänger H.L. An infectious and replicating RNA of low molecular weight: the agent of the exocortis disease of Citrus. Adv. Biosci. 1972, 8:103-116.
10. Lawson R.H. Some properties of chrysanthemum stunt virus. Phytopathology 1968, 58:885.
11. Diener T.O. The Viroids 1987, Plenum Press, New York.
12. Viroids 2003, CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
13. Bar-Joseph M. Natural history of viroids - horticultural aspects. Viroids 2003, 246-251. CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
14. Verhoeven J.Th.J., Jansen C.C.C., Willemen T.M., Kox L.F.F., Owens R.A., Roenhorst J.W. Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid, Potato spindle tuber viroid, and Tomato chlorotic dwarf viroid. Eur. J. Plant Pathol. 2004, 110:823-831.
15. Ling K., Li R., Panthee D.R., Gardner R.G. First report of potato spindle tuber viroid naturally infecting greenhouse tomatoes in North Carolina. Plant Dis. 2013, 97:148.
16. Mathews D.M. Viruses and viroids as invasive plant pathogens. California Ornamental Research Federation (CORF) News, vol. 13, Issue 1 (winter/spring) 2009, 1 and 4 pp. Available at: http://ucanr.org/sites/UCNFA/newsletters/Volume_13,_Issue_121661.pdf.
17. Hammond R.W., Owens R.A. Viroids: new and continuing risks for horticultural and agricultural crops. APSnet Features 2006, 10.1094/APSnetFeature-2006-1106.
18. Di Serio F., Gisel A., Navarro B., Delgado S., Martinez de Alba A.E., Donvito G., Flores R. Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS ONE 2009, 4:e7539.
19. Verhoeven J.Th.J., Jansen C.C.C., Botermans M., Roenhorst J.W. Epidemiological evidence that vegetatively propagated, solanaceous plant species act as sources of Potato spindle tuber viroid inoculum for tomato. Plant Pathol. 2010, 59:3-12.
20. Th J., Verhoeven J., Humer L., Marn M.V., Plessk I.M., Roenhorst J.W. Mechanical transmission of Potato spindle tuber viroid between plants of Brugmansia suaveoles, Solanum jasminoides and potatoes and tomatoes. Eur. J. Plant Pathol. 2010, 128:417-421.
21. Ding B. The biology of viroid-host interactions. Ann. Rev. Phytopathol. 2009, 47:105-131.
22. Riesner D., Gross H.J. Viroids. Annu. Rev. Biochem. 1985, 54:531-564.
23. Tsagris E.M., Martínez de Alba A.E., Gozmanova M., Kalantidis K. Viroids. Cell. Microbiol. 2008, 10:2168-2179.
24. Cho W.K., Jo Y., Jo K.-M., Kim K.H. A current overview of two viroids that infect chrysanthemums: Chrysanthemum stunt viroid and Chrysanthemum chlorotic mottle viroid. Viruses 2013, 5:1099-1113.
25. Flores R., Hernández C., Martínez de Alba A.E., Darós J.A., Di Serio F. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 2005, 43:117-139.
26. Tabler M., Tsagris M. Viroids: petite RNA pathogens with distinguished talents. Trends Plant Sci. 2004, 9:339-348.
27. Prins M., Noris E., Schubert J., Wassenegger M., Tepfer M. Strategies for antiviral resistance in transgenic plants. Mol. Plant Pathol. 2008, 9:73-83.
28. Sano T., Hammond R.W., Owens R.A. Biotechnological approaches for controlling viroid diseases. Viroids 2003, 343-349. CSIRO, Publishing/Science Publishers Inc., Australia/USA. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
29. Sano T., Barba M., Li S.F., Hadidi A. Viroids and RNA silencing: mechanism, role in viroid pathogenicity and development of viroid-resistant plants. GM Crops 2010, 1:80-86.
30. Singh R.P., Randles J.W., Hadidi A. Strategies for the control of viroid diseases. Viroids 2003, 295-302. CSIRO Publishing/Science Publishers Inc., Australia/USA. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
31. Parisi O., Lepoivre P., Jijakli M.H. Plant-RNA viroid relationship: a complex host pathogen interaction. Biotechnol. Agron. Soc. Environ. 2010, 14:461-470.
32. Wu Q., Wang Y., Cao M., Pantaleo V., Burgyan J., Li W.X., Ding S.W. Homology-independent discovery of replicating pathogenic circular RNAs by deep sequencing and a new computational algorithm. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3938-3943.
33. Diener T.O. Origin and evolution of viroids and viroid-like satellite RNAs. Virus Genes 1996, 11:119-131.
34. Diener T.O. The viroid: biological oddity or evolutionary fossil?. Adv. Virus Res. 2001, 57:137-184.
35. Diener T.O. Circular RNAs: relics of precellular evolution?. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:9370-9374.
36. Lai M.M. The molecular biology of hepatitis delta virus. Annu. Rev. Biochem. 1995, 64:259-286.
37. Taylor J.M. Hepatitis delta virus. Intervirology 1999, 42:173-178.
38. Harders J., Lukács N., Robert-Nicoud M., Jovin J.M., Riesner D. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO J. 1989, 8:3941-3949.
39. Owens R.A., Diener T.O. RNA intermediates in potato spindle tuber viroid replication. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:113-117.
40. Branch A.D., Benenfield B.J., Robertson H.D. Evidence for a single rolling circle in the replication of potato spindle tuber viroid. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:9128-9132.
41. Bonfigloili R.G., McFadden G., Symons R.H. In situ hybridization localizes avocado sunblotch viroid in chloroplast thylaloid membranes and coconut cadang cadang viroid in the nucleus. Plant J. 1994, 6:99-103.
42. Hutchins C.J., Rathjen P.D., Forster A.C., Symons R.H. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 1986, 14:3627-3640.
43. Beaudry D., Busiere F., Lareau F., Lessard C., Perreault J.P. The RNA of both polarities of the peach latent mosaic viroid self-cleaves in vitro solely by single hammerhead structures. Nucleic Acids Res. 1995, 23:745-752.
44. Delgado S., Martínez de Alba A.E., Hernández C., Flores R. A short double-stranded RNA motif of Peach latent mosaic viroid contains the initiation and the self-cleavage sites of both polarity strands. J. Virol. 2005, 79:12934-12943.
45. Flores R., Darós J.A., Navarro J.A. Replication. Viroids 2003, 55-60. CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
46. Gross H.J., Domdey H., Lossow C., Jank P., Raba M., Alberty H., Sänger H.L. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 1978, 273:203-208.
47. Sogo J., Koller T., Diener T.O. Potato spindle tuber viroid: X. Visualization and size determination by electron microscopy. Virology 1973, 55:70-80.
48. Sänger H.L., Klotz G., Riesner D., Gross H.J., Kleinschmidt A.K. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc. Natl. Acad. Sci. U. S. A. 1976, 73:3852-3856.
49. Gross H.J., Krupp G., Domdey H., Raba M., Jank P., Lossow C., Alberty H., Ramm K., Sänger H.L. Nucleotide sequence and secondary structure of citrus exocortis and chrysanthemum stunt viroid. Eur. J. Biochem. 1982, 121:249-257.
50. Haseloff J., Symons R.H. Chrysanthemum stunt viroid: primary sequence and secondary structure. Nucleic Acids Res. 1981, 9:2741-2752.
51. Puchta H., Ramm K., Sänger H.L. The molecular structure of hop latent viroid (HLV), a new viroid occurring worldwide in hops. Nucleic Acids Res. 1988, 16:4197-4216.
52. Keese P., Symons R.H. Domains in viroids: evidence of intermolecular RNA rearrangement and their contribution to viroid evolution. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:4582-4586.
53. Flores R., Serra P., Minoia S., Di Serio F., Navarro B. Viroids: from genotype to phenotype just relying on RNA sequence and structure motifs. Front. Microbiol. 2012, 3:217. 10.3389/fmich.2012.00217.
54. Desjardins P.R. Avocado sunblotch. The Viroids 1987, Plenum Press, New York. T.O. Diener (Ed.).
55. Symons R.H. Avocado sunblotch viroid: primary sequence and proposed secondary structure. Nucleic Acids Res. 1981, 9:6527-6537.
56. Flores R., Navarro J.A., de la Peña M., Navarro B., Ambrós S., Vera A. Viroids with hammerhead ribozymes: some unique structural and functional aspects with respect to other members of the group. Biol. Chem. 1999, 380:849-854.
57. Steger G., Riesner D. Molecular characteristics. Viroids 2003, 15-29. CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
58. Zhong X., Leonitis N., Qian S., Itaya A., Qi Y., Boris-Lawrie K., Ding B. Tertiary structural and functional analysis of a viroid RNA motif by isostericity matrix and mutagenesis reveal its essential role in replication. J. Virol. 2006, 80:8566-8581.
59. de la Peña M., Navarro B., Flores R. Mapping of the molecular determinant of pathogenicity in a hammerhead viroid: a tetraloop within the in vivo branched RNA conformation. Proc. Natl Acad. Sci. U. S. A. 1999, 96:9960-9965.
60. Domingo E., Escarmis C., Sevilla N., Moya A., Elena S.F., Quer J., Novella S.I., Holland J.J. Basic concepts in RNA virus evolution. FASEB J. 1996, 10:859-864.
61. Acosta-Leal R., Duffy S., Xiong Z., Hammond R.W., Elena S.F. Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology 2011, 101:1136-1148.
62. Di Serio F., Gisel A., Navarro B., Delgado S., Martínez de Alba A.E., Donvito G., Flores R. Deep sequencing of the small RNAs derived from two symptomatic variants of an chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS ONE 2009, 4:e7539.
63. Gago S., Elena S.E., Flores R., Sanjuàn R. Extremely high mutation rate of a hammerhead viroid. Science 2009, 323:1308.
64. Takeda P., Ding B. Viroid intercellular trafficking: RNA motifs, cellular factors and broad impacts. Viruses 2009, 1:210-221.
65. Zhu Y., Green L., Woo Y.M., Owens R., Ding B. Cellular basis of potato spindle tuber viroid systemic movement. Virology 2001, 279:66-77.
66. Qi Y., Pelisser T., Itaya A., Hunt E., Wassengger M., Ding B. Direct role of a viroid RNA motif in mediating directional RNA trafficking across a cellular boundary. Plant Cell 2004, 16:1741-1752.
67. Palukaitis P. Potato spindle tuber viroid: investigation of the long-distance, intra-plant transport route. Virology 1987, 158:239-241.
68. Zhu Y., Qi Y., Yun Y., Owens R., Ding B. Movement of potato spindle tuber viroid reveals regulatory points of phloem-mediated RNA traffic. Plant Physiol. 2002, 130:138-146.
69. Zhong Y., Tao X., Stombaugh J., Leontis N., Ding B. Tertiary structures and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. EMBO J. 2007, 26:3836-3846.
70. Flores R., Hernández C., Martínez de Alba E., Daròs J.A., Di Serio F. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 2005, 43:117-139.
71. Gómez G., Pallás V. Identification of an in vitro ribonucleoprotein complex between a viroid RNA and a phloem protein from cucumber plants. Mol. Plant Microbe Interact. 2001, 14:910-913.
72. Gómez G., Pallás V. A long distance translocatable phloem protein from cucumber forms a ribonucleoprotein complex in vivo with Hop stunt viroid. J. Virol. 2004, 78:10104-10110.
73. Owens R.A., Blackburn M., Ding B. Possible involvement of the phloem lectin in long-distance viroid movement. Mol. Plant Microbe Interact. 2001, 14:905-909.
74. Bostwick D.E., Skaggs M.I., Thompson G.A. Organization and characterization of Cucurbita phloem lectin genes. Plant Mol. Biol. 1994, 26:887-897.
75. Werner R., Mühlbach H.P., Guitton M.C. Isolation of viroid-RNA-binding proteins from an expression library with nonradioactive-labeled RNA probes. Biotechniques 1995, 19:218-222.
76. Sägesser R., Martinez E., Tsagris M., Tabler M. Detection and isolation of RNA-binding proteins by RNA-ligand screening of a cDNA expression library. Nucleic Acids Res. 1997, 25:3816-3822.
77. Maniataki E., Tabler M., Tsagris M. Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA 2003, 9:346-354.
78. Zhao Y., Owens R.A., Hammond R.W. Use of a vector based on Potato virus X in a whole plant assay to demonstrate nuclear targeting of Potato spindle tuber viroid. J. Gen. Virol. 2001, 82:1491-1497.
79. Abraitiene A., Zhao Y., Hammond R. Nuclear targeting by fragmentation of the Potato spindle tuber viroid genome. Biochem. Biophys. Res. Commun. 2008, 368:470-475.
80. Qi Y., Ding B. Differential subnuclear localization of RNA strands of opposite polarity derived from an autonomously replicating viroid. Plant Cell 2003, 15:2566-2577.
81. Gómez G., Pallás V. Noncoding RNA mediated traffic of foreign mRNA into chloroplasts reveals a novel signaling mechanism in plants. PLoS ONE 2010, 5:e12269.
82. Gómez G., Pallás V. Studies on subcellular compartmentalization of plant pathogenic noncoding RNAs gives new insights into the intracellular RNA-traffic mechanisms. Plant Physiol. 2012, 159:558-564.
83. Martínez de Alba A.E., Sägesser R., Tabler M., Tsagris M. A bromodomain-containing protein from tomato specifically binds potato spindle tuber viroid RNA in vitro and in vivo. J. Virol. 2003, 77:9685-9694.
84. Gozmanova M., Denti M.A., Minkov I.N., Tsagris M., Tabler M. Characterization of the RNA motif responsible for the specific interaction of potato spindle tuber viroid RNA (PSTVd) and the tomato protein Virp1. Nucleic Acids Res. 2003, 31:5534-5543.
85. SenGupta D.J., Zhang B., Kraemer B., Pochart P., Fields S., Wickens M. A three-hybrid system to detect RNA-protein interactions in vivo. Proc. Natl. Acad. Sci. U. S. A 1996, 93:8496-8501.
86. Kalantidis K., Denti M.A., Tzortzakaki S., Marinou E., Tabler M., Tsagris M. Virp1 is a host protein with a major role in potato spindle tuber viroid infection in Nicotiana plants. J. Virol. 2007, 81:12872-12880.
87. Hammond R.W. Agrobacterium-mediated inoculation of PSTVd cDNAs onto tomato reveals the biological effect of apparently lethal mutations. Virology 1994, 201:36-45.
88. Solovyev A.G., Makarova S.S., Remizowa M.V., Lim H.S., Hammond J., Owens R.A., Kopertekh L., Schiemann J., Morozov S.Y. Possible role of the Nt-4/1 protein in macromolecular transport in vascular tissue. Plant Signal Behav. 2013, 8:e25784.
89. Singh R.P. Experimental host range of the potato spindle tuber virus. Am. Potato J. 1973, 50:111-123.
90. Singh R.P. Seed transmission of potato spindle tuber virus in tomato and potato. Am. Potato J. 1970, 47:225-227.
91. Matouŝek J., Orctova L., Skopek J., Pesina K., Steger G. Elimination of hop latent viroid upon developmental activation of pollen nucleases. Biol. Chem. 2008, 389:905-918.
92. Semancik J. Avocado sunblotch viroi. Viroids 2003, 171-177. CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
93. Flores R., Hernandez C., Llacer G., Shamloul A.M., Giunchedi L., Hadidi A. Peach latent mosaic viroid. Viroids 2003, 156-160. CSIRO Publishing, Collingwood, Australia. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
94. Salazar L.F., Querci M., Bartolini I., Lazarte V. Aphid transmission of potato spindle tuber viroid assisted by potato leafroll virus. Fitopatologia 1995, 30:56-58.
95. Querci M., Owens R.A., Bartolini I., Lazarte V., Salazar L.F. Evidence for heterologous encapsidation of potato spindle tuber viroid in particles of potato leafroll virus. J. Gen. Virol. 1997, 78:1207-1211.
96. Syller J., Marczewski W., Pawlowicz J. Transmission by aphids of potato spindle tuber viroid encapsidated by potato leafroll luteovirus particles. Eur. J. Plant Pathol. 1997, 103:285-289.
97. Schumann G.L., Tingey W.M., Thurston H.D. Evaluation of six insect pests for transmission of potato spindle tuber viroid. Am. Potato J. 1980, 57:205-211.
98. Francki R.I.B., Zaitlin M., Palukaitis P. In vivo encapsidation of potato spindle tuber viroid by velvet tobacco mottle virus particles. Virology 1986, 155:469-473.
99. Galindo J., Lopez M., Aguilar T. Significance of Myzus persicae in the spread of tomato plant macho viroid. Fitopatol. Bras. 1986, 11:400-410.
100. Nielsen S.L., Enkegaard A., Nicolaisen A., Kryger P., Marn M.V., Plesko I.M., Kahrer A., Gottsberger R.A. No transmission of Potato spindle tuber viroid shown in experiments with thrips (Frankliniella occidentalis, Thrips tabaci), honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Eur. J. Plant Pathol. 2012, 133:505-509.
101. Matsuura S., Matsushita Y., Kozuka R., Shimizu S., Tsuda S. Transmission of Tomato chlorotic dwarf viroid by bumblebees (Bombus ignites) in tomato plants. Eur. J. Plant Pathol. 2010, 126:111-115.
102. Antignus Y., Lachman O., Pearlsman M. Spread of Tomato apical stunt viroid (TASVd) in greenhouse tomato crops is associated with seed transmission and bumble bee activity. Plant Dis. 2007, 91:47-50.
103. Flores R., Delgado S., Rodio M.E., Ambrós S., Hernández C., Serio F.D. Peach latent mosaic viroid: not so latent. Mol. Plant Pathol. 2006, 7:209-221.
104. O'Brien M.J., Raymer W.B. Symptomless hosts of the potato spindle tuber virus. Phytopathology 1964, 54:1045-1047.
105. Owens R.A., Hammond R. Viroid pathogenicity: one process, many faces. Viruses 2009, 1:298-316.
106. Semancik J.S., Vanderwoude W.J. Exocortis viroid: cytopathic effects at plasma membrane in association with pathogenic RNA. Virology 1976, 69:719-726.
107. Wahn K., Rosenberg-de Gomez F., Sänger H.L. Cytopathic changes in leaf tissue of Gynura aurantiaca infected with the viroid of citrus exocortis disease. J. Gen. Virol. 1980, 49:355-365.
108. Hari V. Ultrastructure of potato spindle tuber viroid-infected tomato leaf tissues. Phytopathology 1980, 70:385-387.
109. Rodio M.E., Delgado S., De Stradis A.E., Gómez M.D., Flores R., Di Serio F. A viroid RNA with a specific structural motif inhibits chloroplast development. Plant Cell 2007, 19:3610-3626.
110. Di Serio F., De Stradis A., Delgado D., Flores R., Navarro B. Cytopathic effects incited by viroid RNAs and putative underlying mechanisms. Front. Plant Sci. 2013, 3:388. 10.3389/fpls.2012.00288.
111. Schnölzer M., Haas B., Ramm K., Hofman H., Sänger H.L. Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J. 1985, 4:2181-2190.
112. Hammond R.W. Analysis of the virulence-modulating region of potato spindle tuber viroid (PSTVd) by site-directed mutagenesis. Virology 1992, 187:654-662.
113. Sano T., Candresse T., Hammond R.W., Diener T.O., Owens R.A. Identification of multiple structural domains regulating viroid pathogenicity. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:10104-10108.
114. Wassenegger M., Spieker R.L., Thalmeir S., Gast F.U., Riedel L. A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 1996, 226:191-197.
115. Qi Y., Ding B. Replication of Potato spindle tuber viroid in cultured cells of tobacco and Nicotiana benthamiana: the role of specific nucleotides in determining replication levels for host adaptation. Virology 2002, 302:445-456.
116. Malfitano M., Di Serio F., Covelli L., Ragozzino A., Hernández C., Flores R. Peach latent mosaic viroid variants including peach calico contain a characteristic insertion that is responsible for this symptomatology. Virology 2003, 313:492-501.
117. Rodio M.E., Delgado S., Flores R., Di Serio F. Variants of peach latent mosaic viroid inducing peach calico: uneven distribution in infected plants and requirements of the insertion containing the pathogenicity determinant. J. Gen. Virol. 2006, 87:231-240.
118. Gadea J., Mayda M.E., Conejero V., Vera P. Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants. Mol. Plant Microbe Interact. 1996, 9:409-415.
119. Camacho Henriquez A., Sänger H.L. Purification and partial characterization of the major pathogenesis-related tomato leaf protein P14 from Potato spindle tuber viroid (PSTVd)-infected tomato leaves. Arch. Virol. 1984, 81:263-284.
120. Itaya A., Matsuda Y., Gonzales R.A., Nelson R.S., Ding B. Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol. Plant Microbe Interact. 2002, 15:990-999.
121. Owens R.A., Tech K.B., Shao J.Y., Sano T., Baker C.J. Global analysis of tomato gene expression during Potato spindle tuber viroid infections reveals a complex array of changes affecting hormone signaling. Mol. Plant Microbe Interact. 2012, 25:582-598.
122. Lisón P., Tárraga S., López-Gresa P., Sauri A., Torres C., Campos L., Bellés J.M., Conejero V., Rodrigo I. A noncoding plant pathogen provokes both transcriptional and posttranscriptional alterations in tomato. Proteomics 2013, 13:833-844.
123. Dubé A., Bisaillon M., Perreault J.P. Identification of proteins from Prunus persica that interact with peach latent mosaic viroid. J. Virol. 2009, 83:12057-12067.
124. Hiddinga H.J., Crum C.J., Hu J., Roth D.A. Viroid-induced phosphorylation of a host protein related to a dsRNA-dependent protein kinase. Science 1988, 241:451-453.
125. Crum C.J., Hu J., Hiddinga H.J., Roth D.A. Tobacco mosaic virus infection stimulates the phosphorylation of a plant protein associated with double-stranded RNA-dependent protein kinase activity. J. Biol. Chem. 1988, 263:13440-13443.
126. Diener T.O., Hammond R.W., Black T., Katze M.G. Mechanism of viroid pathogenesis: differential activation of the interferon-induced, double-stranded RNA-activated, Mr 68,000 protein kinase by viroid strains of varying pathogenicity. Biochimie 1993, 75:533-538.
127. Hammond R.W., Zhao Y. Characterization of a tomato protein kinase gene induced by infection by Potato spindle tuber viroid. Mol. Plant Microbe Interact. 2000, 13:903-910.
128. Wassenegger M., Heimes S., Riedel L., Sänger H.L. RNA-directed de novo methylation of genomic sequences in plants. Cell 1994, 76:567-576.
129. Martínez de Alba A.E., Flores R., Hernández C. Two chloroplastic viroids induce the accumulation of small RNAs associated with post-transcriptional gene silencing. J. Virol. 2002, 76:13094-13096.
130. Markarian N., Li H.E., Ding S.W., Semancik J.S. RNA silencing as related to viroid-induced symptom expression. Arch. Virol. 2004, 149:397-406.
131. Diermann N., Matouŝek J., Junge M., Riesner D., Steger G. Characterization of plant miRNAs and small RNAs derived from potato spindle tuber viroid (PSTVd) infected tomato. Biol. Chem. 2010, 391:1379-1390.
132. Papaefthimiou I., Hamilton A., Denti M., Baulcombe D., Tsagris M., Tabler M. Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res. 2001, 29:2395-2400.
133. Sano T., Matsuura Y. Accumulation of short interfering RNAs characteristic of RNA silencing precedes recovery of tomato plants from severe symptoms of Potato spindle tuber viroid infection. J. Gen. Plant Pathol. 2004, 70:50-53.
134. Gómez G., Martínez G., Pallás V. Interplay between viroid-induced pathogenesis and RNA silencing pathways. Trends Plant Sci. 2009, 14:264-269.
135. Itaya A., Folimonov A., Matsuda Y., Nelson R.S., Ding B. Potato spindle tuber viroid as inducer of RNA silencing in infected tomato. Mol. Plant Microbe Interact. 2001, 14:1332-1334.
136. Itaya A., Zhong X., Bundschuh R., Qi Y., Takeda Y.R., Harris A.R., Molina C., Nelson R.S., Ding B. A structured viroid RNA serves as a substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complex-mediated degradation. J. Virol. 2007, 81:2980-2994.
137. Wang Y., Shibuya M., Taneda A., Kurauchi T., Senda M., Owens R.A., Sano T. Accumulation of Potato spindle tuber viroid-specific RNAs is accompanied by specific changes in gene expression in two tomato cultivars. Virology 2011, 413:72-83.
138. Di Serio F., Martínez de Alba A.E., Nabarro B., Gisel A., Flores R. RNA-dependent RNA polymerase 6 delays accumulation and precludes meristem invasion of a viroid that replicates in the nucleus. J. Virol. 2010, 84:2477-2489.
139. Martínez G., Castellano M., Tortosa M., Pallás V., Gómez G. A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Res. 2014, 42:1553-1562.
140. Di Serio F., Gisel A., Navarro B., Delgado S., Martínez de Alba A.-E., Donvito G., Flores R. Deep sequencing of the small RNAs derived from two symptomatic variants of a chloroplastic viroid: implications for their genesis and for pathogenesis. PLoS ONE 2009, 4(10):e7539. 10.1371/journal.pone.0007539.2009.
141. Machida S., Yamahata N., Watanuki H., Owens R.A., Sano T. Successive accumulation of two size classes of viroid-specific small RNA in potato spindle tuber viroid-infected tomato plants. J. Gen. Virol. 2007, 88:3452-3457.
142. Gómez G., Pallás V. Mature monomeric forms of Hop stunt viroid resist RNA silencing in transgenic plants. Plant J. 2007, 51:1041-1049.
143. Schwind N., Zwiebel M., Itaya A., Ding B., Wang M-B., Krczal G., Wassenegger M. RNAi-mediated resistance to Potato spindle tuber viroid in transgenic tomato expressing a viroid hairpin RNA construct. Mol. Plant Pathol. 2009, 10:459-469.
144. Singh R.P., Slack S.A. Reactions of tuber-bearing Solanum species to infection with potato spindle tuber viroid. Plant Dis. 1984, 68:784-787.
145. Singh R.P. Clones of Solanum berthaultii resistant to potato spindle tuber viroid. Phytopathology 1985, 75:1432-1434.
146. Singh R.P. A local lesion host for potato spindle tuber virus. Phytopathology 1971, 61:1034-1035.
147. Salazar L.F., Hammond R.W., Diener T.O., Owens R.A. Analysis of viroid replication following Agrobacterium-mediated inoculation of non-host species with potato spindle tuber viroid cDNA. J. Gen. Virol. 1988, 69:879-889.
148. Harris P.S., Miller-Jones D.M., Howell P.J. Control of potato spindle tuber viroid: the special problems of a disease in plant breeders' material. Plant Health: The Scientific Basis for Administrative Control of Plant Parasites 1979, 232-237. Blackwell, Oxford, England. D.L. Ebbels, J.E. King (Eds.).
149. Pfannenstiel M.A., Slack S.A. Response of potato cultivars to infection by potato spindle tuber viroid. Phytopathology 1980, 70:922-926.
150. Omori H., Hosokawa M., Shiba H., Shitsukawa N., Murai K., Yazawa S. Screening of chrysanthemum plants with strong resistance to Chrysanthemum stunt viroid. J. Jpn. Soc. Hortic. Sci. 2009, 78:350-355.
151. Matsushita Y., Aoki K., Sumitomo K. Selection and inheritance of resistance to Chrysanthemum stunt viroid. Crop Prot. 2012, 35:1-4.
152. Heath M.C. Tansley Review No. 33. Evolution of resistance to fungal parasitism in natural ecosystems. New Phytol. 1991, 119:331-343.
153. Thordal-Christensen H. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 2003, 6:351-357.
154. Ellis J. Insights into nonhost disease resistance: can they assist disease control in agriculture. Plant Cell 2006, 18:523-528.
155. Schulze-Lefert P., Panstruga R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 2011, 16:117-125.
156. Daròs J.A., Flores R. Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6792-6797.
157. Barba M., Gumpf D.J., Hadidi A. Quarantine of imported germplasm. Viroids 2003, 303-311. CSIRO Publishing/Science Publishers Inc., Australia/USA. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
158. Raymer W.B., O'Brien M.J. Transmission of potato spindle tuber virus to tomato. Am. Potato J. 1962, 39:401-408.
159. Schumacher J., Meyer N., Riesner D., Weiderman H.L. Diagnostic procedure for detection of viroids and viruses with circular RNAs by 'return'-gel electrophoresis. J. Phytopathol. 1986, 115:332-343.
160. Hammond R., Smith D.R., Diener T.O. Nucleotide sequence and proposed secondary structure of Columnea latent viroid: a natural mosaic of viroid sequences. Nucleic Acids Res. 1989, 17:10083-10094.
161. Owens R.A., Diener T.O. Sensitive and rapid diagnosis of potato spindle tuber viroid disease by nucleic acid hybridization. Science 1981, 213:670-672.
162. Bostan H., Nie X., Singh R.P. An RT-PCR primer pair for the detection of Pospiviroid and its application in surveying ornamental plants for viroids. J. Virol. Methods 2004, 116:189-193.
163. Botermans M., van de Vossenberg B.T., Verhoeven J.T., Roenhorst J.W., Hoofman M., Dekter R., Meekes E.T. Development and validation of a real-time RT-PCR assay for generic detection of pospiviroids. J. Virol. Methods 2013, 187:43-50.
164. De Boer S.H., DeHaan T.L. Absence of Potato spindle tuber viroid within the Canadian potato industry. Plant Dis. 2005, 89:210.
165. Singh R.P., Crowley C.F. Evaluation of polyacrylamide gel electrophoresis, bioassay, and dot-blot methods for the survey of potato spindle tuber viroid. Can. Plant Dis. Surv. 1985, 65:61-63.
166. Barba M., Czonek H., Hadidi A. Historical perspective, development and applications of next-generation sequencing in plant virology. Viruses 2014, 6:106-136.
167. Zhang Y., Yin J., Jiang D., Xin Y., Ding F., Deng Z., Wang G., Ma X., Li F., Li G., Li M., Li S., Zhu S. A universal oligonucleotide array with a minimal number of probes for the detection and identification of viroids at the genus level. PLoS ONE 2013, 8:e64474.
168. Garnsey S.M., Whidden R. Decontamination treatments to reduce the spread of citrus exocortis (CEVd) by contaminated tools. Proc. Fla. Stn. Hortic. Soc. 1972, 84:63-65.
169. Roistacher C.N., Calavan E.C., Blue R.L. Citrus exocortis virus - chemical inactivation on tools, tolerance to heat and separation of isolates. Plant Dis. Rep. 1969, 53:333-336.
170. Singh R.P., Boucher A., Somerville T.H. Evaluation of chemicals for disinfection of laboratory equipment exposed to potato spindle tuber viroid. Am. Potato J. 1989, 66:239-246.
171. Singh R.P. Piperonyl butoxide as a protectant against Potato spindle tuber viroid infection. Dis. Control Pest Manage. 1977, 67:933-935.
172. Bellés J.M., Hansen A.J., Granell A., Conejero V. Antiviroid effect of ribavirin on citrus exocortis viroid infection in Gynura aurantiaca DC. Physiol. Mol. Plant Pathol. 1986, 28:61-65.
173. Barba M., Ragozzino E., Navarro L. Viroid elimination by thermotherapy and tissue culture. Viroids. 2003, 318-323. CSIRO Publishing/Science Publishers Inc., Australia/USA. A. Hadidi, R. Flores, J.W. Randles, J.S. Semancik (Eds.).
174. Chung B.N., Huh E.J., Kim J.S. Effect of temperature on the concentration of Chrysanthemum stunt viroid in CSVd-infected chrysanthemum. Plant Pathol. J. 2006, 22:152-154.
175. El-Dougdoug Kh.A., Osman M.E., Abdelkader H.S., Dawoud R.A., Elbaz R.M. Elimination of Hop stunt viroid (HSVd) from infected peach and pear plants using cold therapy and chemotherapy. Aust. J. Basic Appl. Sci. 2010, 4:54-60.
176. Matousek J., Trněná L., Svoboda P., Oriniaková P., Lichtenstein C.P. The gradual reduction of viroid levels in hop mericlones following heat therapy: a possible role for a nuclease degrading dsRNA. Biol. Chem. Hoppe Seyler 1995, 376:715-721.
177. Mahfouze S.A., El-Dougdoug Kh.A., Allam E.K. Production of Potato spindle tuber viroid-free potato plant materials in vitro. N. Y. Sci. J. 2010, 60-67.
178. Hollings M., Stone O.M. Attempts to eliminate chrysanthemum stunt from chrysanthemum by meristem-tip culture after heat treatment. Ann. Appl. Biol. 1970, 65:311-315.
179. Lizárraga R.E., Salazar S.F., Roca W.M., Schilde-Rentschler L. Elimination of potato spindle tuber viroid by low temperature and meristem culture. Phytopathology 1980, 70:754-755.
180. Paduch-Cichal E., Kryczyński S. A low temperature therapy and meristem-tip culture for eliminating four viroids from infected plants. J. Phytopathol. 1987, 118:341-346.
181. Postman J., Hadidi A. Elimination of apple scar skin viroid from pears by in vitro thermotherapy and apical meristem culture. Acta Hortic. 1995, 386:536-543.
182. Adams A.N., Barbara G.J., Morton A., Darby P. The experimental transmission of hop latent viroid and its elimination by low temperature treatment and meristem culture. Ann. Appl. Biol. 1996, 128:37-44.
183. Jeon S-M., Savitri W.D., Park K-I., Chung M-Y., Kim C-K. Elimination of Chrysanthemum stunt viroid (CSVd) from a viroid-infected chrysanthemum through shoot tip culture. Flower Res. J. 2012, 20:218-222.
184. Savitri W.D., Park K.I., Jeon S.M., Chung M.Y., Han J-S., Kim C.K. Elimination of Chrysanthemum stunt viroid (CSVd) from meristem tip culture combined with prolonged cold treatment. Hortic. Environ. Biotechnol. 2013, 54:177-182.
185. Wang Q., Valkonen J.P.T. Cryotherapy of shoot tips: novel pathogen eradication method. Trends Plant Sci. 2009, 14:119-122.
186. Navarro L., Llácer G., Cambra M., Arregui J.M., Juárez J. Shoot-tip grafting in vitro for elimination of viruses in peach plants (Prunus persica Batsch). Acta Hortic. 1983, 130:185-192.
187. Navarro L. Citrus shoot tip grafting in vitro. Biotechnology in Agriculture and Forestry. High-Tech and Micropropagation 1992, 327-338. Springer-Verlag, Berlin. J.P.S. Bajaj (Ed.).
188. Nel M., de Lange J. Shoot tip grafting of avocado for virus and viroid elimination. S. Afr. Avocado Grow. Assoc. Yearb. 1985, 8:66-69.
189. Kapari-Isaia Th., Minas G.J., Polykarpou D., Iosephidou E., Arseni Sp., Kyriakou A. Shoot-tip grafting in vitro for elimination of viroids and Citrus psorosis virus in the local Arakapas Mandarin in Cyprus. Proceedings of the 15th IOCV Conference 2002, 417-420.
190. Hosokawa M., Otake A., Sugawara Y., Hayashi T., Yazawa S. Rescue of shoot apical meristems of chrysanthemum by culturing on root tips. Plant Cell Rep. 2004, 22:443-448.
191. Hosokawa M., Otake A., Ohishi K., Ueda E., Hayashi T., Yazawa S. Elimination of Chrysanthemum stunt viroid from an infected chrysanthemum cultivar by shoot regeneration from a leaf primordium-free shoot apical meristem dome attached to a root tip. Plant Cell Rep. 2004, 22:859-863.
192. Hosokawa M., Matsushita Y., Ohishi K., Yazawa S. Elimination of Chrysanthemum chlorotic mottle viroid (CChMVd) recently detected in Japan by leaf-primordia free shoot apical meristem culture from infected cultivars. J. Jpn. Soc. Hortic. Sci. 2005, 74:386-391.
193. Horst R.K., Cohen D. Amantadine supplement tissue culture medium: a method for obtaining chrysanthemum free of chrysanthemum stunt viroid. Acta Hortic. 1980, 110:315-319.
194. Lozoya-Saldaña H., Abelló J.F., de la G., García R. Electrotherapy and shoot tip culture eliminate potato virus X in potatoes. Am. Potato J. 1996, 73:149-154.
195. Meybodi D.E., Mozafari J., Babaeiyan N., Rahimian H. Application of electrotherapy for the elimination of potato potyviruses. J. Agric. Sci. Technol. 2011, 13:921-927.
196. McKinney H.H. Mosaic diseases in the Canary Islands, West Africa and Gibraltar. J. Agric. Res. 1929, 39:557-578.
197. Fernow K.H. Tomato as a test plant for detecting mild strains of potato spindle tuber virus. Phytopathology 1967, 57:1347-1352.
198. Niblett C.L., Dickson E., Fernow K.H., Horst R.K., Zaitlin M. Cross protection among four viroids. Virology 1978, 91:198-203.
199. Branch A.D., Benenfeld B.J., Franck E.R., Shaw J.F., Varban M.L., Willis K.K., Rosen D.L., Robertson H.D. Interference between co-inoculated viroids. Virology 1988, 163:538-546.
200. Singh R.P., Boucher A., Somerville T.H. Cross-protection with strains of Potato spindle tuber viroid in the potato plant and other Solanaceous hosts. Phytopathology 1990, 80:246-250.
201. Hull R. Matthews' Plant Virology 2004, Elsevier, Academic Press, London, United Kingdom. fourth ed.
202. Lin S.S., Henriques R., Wu H.W., Niu Q.W., Yeh S.D., Chua N.H. Strategies and mechanisms of plant virus resistance. Plant Biotechnol. Rep. 2007, 1:125-134.
203. Sherwood J.L. Mechanisms of cross-protection between plant virus strains. Plant Resistance to Viruses 1987, 136-150. Wiley, Chichester, UK. D. Evered, S. Harnett (Eds.).
204. Zhou C.Y., Hailstones D.L., Broadbent P., Connor R., Bowyer J. Studies on mild strain cross protection against stem-pitting tristeza virus. Proceedings of the 15th Conference on IOCV, IOCV 2002, 151U-157U.
205. Ratcliff F.G., MacFarlane S.A., Baulcombe D.C. Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 1999, 11:1207-1215.
206. Zhou C., Zhou Y. Strategies for viral cross protection in plants. Methods Mol. Biol. 2012, 894:69-81.
207. Costa A.S., Müller G.W. Tristeza controlled by cross protection, a US-Brazil cooperative success. Plant Dis. 1980, 64:538-541.
208. Danna C.H., Millet Y.A., Koller T., Han S-W., Bent A.F., Ronald P.C., Ausubel F.M. The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9286-9291.
209. Lee S-W., Sang-Wook Han S-W., Sririyanum M., Park C-J., Seo Y-S., Ronald P.C. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 2009, 326:850-853.
210. Sun X., Cao Y., Yang Z., Xu C., Li X., Wang S., Zhang Q. Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J. 2004, 37:517-527.
211. Nagaveni V., Mahadeva A., Sreevathsa R. Plants under attack: phytoalexins in defense mechanism. Genetically Engineered Crops: Biotechnology, Biosafety and Benefits 2011, 193-209. Nova Science Publishers, New York. L.M. Grover (Ed.).
212. Zurbriggen M.D., Carrillo N., Hajirezaei M-R. ROS signaling in the hypersensitive response: when, where and what for?. Plant Signal. Behav. 2010, 5:393-396.
213. Morel J-B., Dangl J.L. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 1997, 4:671-683.
214. Baulcombe D. RNA silencing in plants. Nature 2004, 431:356-363.
215. Matousek J., Schröder A.R.W., Trněná L., Reimers M., Baumstark T., Dědic P., Vlasák J., Becker I., Kreuzaler F., Fladung M., Riesner D. Inhibition of viroid infection by antisense RNA expression in transgenic plants. Biol. Chem. Hoppe Seyler 1994, 375:765-777.
216. Atkins D., Young M., Uzzell S., Kelly L., Fillatti J., Gerlach W.L. The expression of antisense and ribozyme genes targeting citrus exocortis viroid in transgenic plants. J. Gen. Virol. 1995, 76:1781-1790.
217. Yang X., Yie Y., Zhu F., Liu Y., Kang L., Wang X., Tien P. Ribozyme-mediated high resistance against potato spindle tuber viroid in transgenic potatoes. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4861-4865.
218. Carbonell A., Flores R., Gago S. Hammerhead ribozymes against virus and viroid RNAs. From Nucleic Acid Sequences to Molecular Medicine, RNA Technologies 2012, 411-427. Springer-Verlag, Berlin Heidelberg. V.A. Erdmann, J. Barciszewski (Eds.).
219. Carbonell A., Flores R., Gago S. Trans-cleaving hammerhead ribozymes with tertiary stabilizing motifs: in vitro and in vivo activity against a structured viroid RNA. Nucleic Acids Res. 2011, 39:2432-2444.
220. Hernández C., Flores R. Plus and minus RNAs of peach latent mosaic viroid self-cleave in vitro via hammerhead structures. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:3711-3715.
221. Uhlenbeck O.C. A small catalytic oligonucleotide. Nature 1987, 328:596-600.
222. Saksmerprome V., Roychowdhury-Saha M., Jayasena S., Khvorova A., Burke D.H. Artificial tertiary motifs stabilize trans-cleaving hammerhead ribozymes under conditions of submillimolar divalent ions and high temperatures. RNA 2004, 10:1916-1924.
223. Weinberg M.S., Rossi J.J. Comparative single-turnover kinetic analyses of trans-cleaving hammerhead ribozymes with naturally derived non-conserved sequence motifs. FEBS Lett. 2005, 579:1619-1624.
224. Gómez G., Martínez G., Pallás V. Viroid-induced symptoms in Nicotiana benthamiana plants are dependent on RDR6 activity. Plant Physiol. 2008, 148:414-423.
225. Kasai A., Bai S., Li T., Harada T. Graft-transmitted siRNA signal from the root induces visual manifestation of endogenous post-transcriptional gene silencing in the scion. PLoS ONE 2011, 6:e16895.
226. Kasai A., Sano T., Harada T. Scion on a stock producing siRNAs of potato spindle tuber viroid (PSTVd) attenuates accumulation of the viroid. PLoS ONE 2013, 8:e57736.
227. Carbonell A., Martínez de Alba A.E., Flores R., Gago S. Double-stranded RNA interferes in a sequence-specific manner with the infection of representative members of the two viroid families. Virology 2008, 371:44-53.
228. Rotondo G., Frendewey D. Purification and characterization of the Pac1 ribonuclease of Schizosaccharomyces pombe. Nucleic Acids Res. 1996, 24:2377-2386.
229. Watanabe Y., Ogawa T., Takahashi H., Ishida I., Takeuchi Y., Yamamoto M., Okada Y. Resistance against multiple plant viruses in plants mediated by a double stranded-RNA specific ribonuclease. FEBS Lett. 1995, 372:165-168.
230. Ishida I., Tukahara M., Yoshioka M., Ogawa T., Kakitani M., Toguri T. Production of anti-virus, viroid plants by genetic manipulations. Pest Manage. Sci. 2002, 58:1132-1136.
231. Ogawa T., Toguri T., Kudoh H., Okamura M., Momma T., Yoshioka M., Kato K., Hagiwara Y., Sano T. Double-stranded RNA-specific ribonuclease confers tolerance against Chrysanthemum stunt viroid and Tomato spotted wilt virus in transgenic chrysanthemum plants. Breed. Sci. 2005, 55:49-55.
232. Sano T., Nagayama A., Ogawa T., Ishida I., Okada Y. Transgenic potato expressing a double-stranded RNA-specific ribonuclease is resistant to potato spindle tuber viroid. Nat. Biotechnol. 1997, 15:1290-1294.